Evolutionary Biologist; Emeritus Professor of the Public Understanding of Science, Oxford; Author, The Greatest Show on Earth, The Magic of Reality

A flip-flop should be no handicap

When a politician changes his mind, he is a 'flip-flopper.' Politicians will do almost anything to disown the virtue — as some of us might see it — of flexibility. Margaret Thatcher said, "The lady is not for turning." Tony Blair said, "I don't have a reverse gear." Leading Democratic Presidential candidates, whose original decision to vote in favour of invading Iraq had been based on information believed in good faith but now known to be false, still stand by their earlier error for fear of the dread accusation: 'flip-flopper'. How very different is the world of science. Scientists actually gain kudos through changing their minds. If a scientist cannot come up with an example where he has changed his mind during his career, he is hidebound, rigid, inflexible, dogmatic! It is not really all that paradoxical, when you think about it further, that prestige in politics and science should push in opposite directions.

I have changed my mind, as it happens, about a highly paradoxical theory of prestige, in my own field of evolutionary biology. That theory is the Handicap Principle suggested by the Israeli zoologist Amotz Zahavi. I thought it was nonsense and said so in my first book, The Selfish Gene. In the Second Edition I changed my mind, as the result of some brilliant theoretical modelling by my Oxford colleague Alan Grafen.

Zahavi originally proposed his Handicap Principle in the context of sexual advertisement by male animals to females. The long tail of a cock pheasant is a handicap. It endangers the male's own survival. Other theories of sexual selection reasoned — plausibly enough — that the long tail is favoured in spite of its being a handicap. Zahavi's maddeningly contrary suggestion was that females prefer long tailed males, not in spite of the handicap but precisely because of it. To use Zahavi's own preferred style of anthropomorphic whimsy, the male pheasant is saying to the female, "Look what a fine pheasant I must be, for I have survived in spite of lugging this incapacitating burden around behind me."

For Zahavi, the handicap has to be a genuine one, authentically costly. A fake burden — the equivalent of the padded shoulder as counterfeit of physical strength — would be rumbled by the females. In Darwinian terms, natural selection would favour females who scorn padded males and choose instead males who demonstrate genuine physical strength in a costly, and therefore, unfakeable way. For Zahavi, cost is paramount. The male has to pay a genuine cost, or females would be selected to favour a rival male who does so.

Zahavi generalized his theory from sexual selection to all spheres in which animals communicate with one another. He himself studies Arabian Babblers, little brown birds of communal habit, who often 'altruistically' feed each other. Conventional 'selfish gene' theory would seek an explanation in terms of kin selection or reciprocation. Indeed, such explanations are usually right (I haven't changed my mind about that). But Zahavi noticed that the most generous babblers are the socially dominant individuals, and he interpreted this in handicap terms. Translating, as ever, from bird to human language, he put it into the mouth of a donor bird like this: "Look how superior I am to you, I can even afford to give you food." Similarly, some individuals act as 'sentinels', sitting conspicuously in a high tree and not feeding, watching for hawks and warning the rest of the flock who are therefore able to get on with feeding. Again eschewing kin selection and other manifestations of conventional selfish genery, Zahavi's explanation followed his own paradoxical logic: "Look what a great bird I am, I can afford to risk my life sitting high in a tree watching out for hawks, saving your miserable skins for you and allowing you to feed while I don't." What the sentinel pays out in personal cost he gains in social prestige, which translates into reproductive success. Natural selection favours conspicuous and costly generosity.

You can see why I was sceptical. It is all very well to pay a high cost to gain social prestige; maybe the raised prestige does indeed translate into Darwinian fitness; but the cost itself still has to be paid, and that will wipe out the fitness gain. Don't evade the issue by saying that the cost is only partial and will only partially wipe out the fitness gain. After all, won't a rival individual come along and out-compete you in the prestige stakes by paying a greater cost? And won't the cost therefore escalate until the point where it exactly wipes out the alleged fitness gain?

Verbal arguments of this kind can take us only so far. Mathematical models are needed, and various people supplied them, notably John Maynard Smith who concluded that Zahavi's idea, though interesting, just wouldn't work. Or, to be more precise, Maynard Smith couldn't find a mathematical model that led to the conclusion that Zahavi's theory might work. He left open the possibility that somebody else might come along later with a better model. That is exactly what Alan Grafen did, and now we all have to change our minds.

I translated Grafen's mathematical model back into words, in the Second Edition of The Selfish Gene (pp 309-313), and I shall not repeat myself here. In one sentence, Grafen found an evolutionarily stable combination of male advertising strategy and female credulity strategy that turned out to be unmistakeably Zahavian. I was wrong to dismiss Zahavi, and so were a lot of other people.

Nevertheless, a word of caution. Grafen's role in this story is of the utmost importance. Zahavi advanced a wildly paradoxical and implausible idea, which — as Grafen was able to show — eventually turned out to be right. But we must not fall into the trap of thinking that, therefore, the next time somebody comes up with a wildly paradoxical and implausible idea, that one too will turn out to be right. Most implausible ideas are implausible for a good reason. Although I was wrong in my scepticism, and I have now changed my mind, I was still right to have been sceptical in the first place! We need our sceptics, and we need our Grafens to go to the trouble of proving them wrong.